Nitrogen Nutrition Promotes Rhizome Bud Outgrowth via Regulation of Cytokinin Biosynthesis Genes and an Oryza longistaminata Ortholog of FINE CULM 1

Shibasaki, Kazuo; Takebayashi, Arika; Makita, Naomasa; Kojima, Mikiko; Takebayashi, Yumiko; Kawai, Misako; Hachiya, Takushi; Sakakibara, Hitoshi

doi:10.3389/fpls.2021.670101

Cited by 15 publications

(17 citation statements)

References 30 publications

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“…Previous studies in O. sativa and O. longistaminata indicated that NADH-GOGAT1 is under the same control as IPT4 in the local nitrogen response and that glutamine-related signaling is involved in the regulation ( Kamada-Nobusada et al, 2013 ; Ohashi et al, 2017 ; Shibasaki et al, 2021 ). OlNADH-GOGAT2 , an isogene, is compensatively upregulated in our experimental conditions, whereas OlNADH-GOGAT1 had a similar expression pattern to OlIPT4 ( Supplemental Figure S7 ).…”

Section: Discussionmentioning

confidence: 98%

“…Oryza longistaminata is a wild rice species that preferentially grows in wetlands and vegetatively reproduces through rhizome growth that can be so vigorous as to occupy an area completely ( Vaughan, 1994 ). Rhizome growth is characterized by the underground horizontal outgrowth of axillary buds to form new rhizomes that expand into new territory ( Yoshida et al, 2016 ; Fan et al, 2017 ; Kyozuka, 2017 ; Bessho-Uehara et al, 2018 ; Toriba et al, 2020 ; Shibasaki et al, 2021 ). Rhizome tips developmentally transform into photosynthetic above-ground organs by growing into a new plantlet called a ramet.…”

Section: Introductionmentioning

confidence: 99%

“…In O. sativa , a glutamine-related signal stimulates OsIPT4 and OsIPT5 expression that are involved in axillary bud outgrowth from shoots ( Kamada-Nobusada et al, 2013 ; Ohashi et al, 2017 ). In O. longistaminata , the outgrowth of rhizome axillary buds in response to nitrogen nutrition is regulated by a similar process to that of the axillary shoot bud in O. sativa , despite differences in the physiological roles of these organs ( Shibasaki et al, 2021 ). In contrast, strigolactone is involved in the nutrient-responsive suppression of shoot axillary bud outgrowth ( Gomez-Roldan et al, 2008 ; Umehara et al, 2008 ; Minakuchi et al, 2010 ; Umehara et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

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Regulation of ammonium acquisition and use in Oryza longistaminata ramets under nitrogen source heterogeneity

et al. 2022

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Oryza longistaminata, a wild rice, vegetatively reproduces and forms a networked clonal colony consisting of ramets connected by rhizomes. Although water, nutrients, and other molecules can be transferred between ramets via the rhizomes, inter-ramet communication in response to spatially heterogeneous nitrogen availability is not well understood. We studied the response of ramet pairs to heterogeneous nitrogen availability using a split hydroponic system that allowed each ramet root to be exposed to different conditions. Ammonium uptake was compensatively enhanced in the sufficient-side root when roots of the ramet pairs were exposed to ammonium-sufficient and -deficient conditions. Comparative transcriptome analysis revealed that a gene regulatory network for effective ammonium assimilation and amino acid biosynthesis was activated in the sufficient-side roots. Allocation of absorbed nitrogen from the nitrogen-sufficient to the -deficient ramets was rather limited. Nitrogen was preferentially used for newly growing axillary buds on the sufficient-side ramets. Biosynthesis of trans-zeatin, a cytokinin, was up-regulated in response to the nitrogen supply, but trans-zeatin appeared not to target the compensatory regulation. Our results also implied that the O. longistaminata putative ortholog of rice (Oryza sativa) C-terminally encoded peptide1 (OsCEP1) plays a role as a nitrogen-deficient signal in inter-ramet communication, providing compensatory up-regulation of nitrogen assimilatory genes. These results provide insights into the molecular basis for efficient growth strategies of asexually proliferating plants growing in areas where the distribution of ammonium ions is spatially heterogeneous.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Regulation of ammonium acquisition and use in Oryza longistaminata ramets under nitrogen source heterogeneity

et al. 2022

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“…In the case of hormone-mediated signaling pathway and IBA, upregulation of genes IPT5, CKX4, and LOGL1 and downregulated genes CKX5, LOG, and LOGL10 in the cytokinin metabolic process. Several previous studies discussed these genes in plant development in different plants ( Kurakawa et al, 2007 ; Ramirez-Carvajal et al, 2009 ; Böttcher et al, 2015 ; Wang et al, 2020 ; Shibasaki et al, 2021 ), and Cytokinin has been known to be a negative regulator of adventitious rooting via its negative regulation of auxin ( Ramirez-Carvajal et al, 2009 ; Li et al, 2016b ). The two downregulated genes, ACC1 and ACS7 of the 1-aminocyclopropane-1-carboxylate metabolic process, need to understand more in the case of sugarcane.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome Analysis Reveals a Gene Expression Pattern That Contributes to Sugarcane Bud Propagation Induced by Indole-3-Butyric Acid

Deng

et al. 2022

Front. Plant Sci.

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Sugarcane is a cash crop that plays an integral part in the sugar industry. The Sustainable Sugarcane Initiative (SSI) has been adopted globally, ensuring enough and aiming for more yield, helping increase disease-free sugarcane cultivation. Single-bud seeds could be the best approach for sugarcane cultivation. Indole-3-butyric acid (IBA) is a rooting agent utilized significantly in seedling propagation. Greenhouse experiment results discovered the significant growth promotion in sugarcane seedlings and accumulation of plant hormones at 100 ppm IBA. Next, we performed transcriptomic analysis of sugarcane buds using RNA sequencing and compared their gene expression during root development due to affect of IBA (100 ppm). A total of 113,475 unigenes were annotated with an average length of 836 bp (N50 = 1,536). The comparative RNA-seq study between the control (CK) and IBA-treated (T) buds showed significant differentially expressed unigenes (494 upregulated and 2086 downregulated). The IBA influenced major biological processes including metabolic process, the cellular process, and single-organism process. For cellular component category, cell, cell part, organelle, membrane, and organelle part were mainly affected. In addition, catalytic activity and binding were primarily affected in the molecular function categories. Furthermore, the expression of genes related to plant hormones and signaling pathways was analyzed by qRT-PCR, which was consistent with the RNA-seq expression profile. This study provides new insights into the IBA response to the bud sprouting in sugarcane based on RNA sequencing, and generated information could help further research on breeding improvement of sugarcane.

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“…Nitrogen nutrition is one of the major environmental factors regulating CK biosynthesis, including tZ-type CK biosynthesis, for plant growth optimization (Takei et al, 2001b;Kamada-Nobusada et al, 2013;Ohashi et al, 2017;Osugi et al, 2017;Maeda et al, 2018;Sakakibara, 2021;Shibasaki et al, 2021;Kawai et al, 2022).…”

Section: Regulation Of Cyp735a3 and Cyp735a4 Expression By Nitrogen S...mentioning

confidence: 99%

Thetrans-zeatin-type side-chain modification of cytokinins controls rice growth

Kiba

Mizutani

Nakahara

et al. 2022

Preprint

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Cytokinins (CKs), a class of phytohormones with vital roles in growth and development, occur naturally with various side-chain structures, including N6-(?2-isopentenyl)adenine-, cis-zeatin- and trans-zeatin (tZ)-types. Recent studies in a model dicot plant Arabidopsis demonstrated that tZ-type CKs are biosynthesized via cytochrome P450 monooxygenase (P450) CYP735A, and have a specific function in shoot growth promotion. Although the function of some of these CKs has been demonstrated in a few dicotyledonous plant species, the significance of these variations and their biosynthetic mechanism and function in monocots and in plants with distinctive side-chain profiles than Arabidopsis, such as Oryza sativa (rice), remain elusive. In this study, we characterized CYP735A3 and CYP735A4 to investigate the role of tZ-type CKs in rice. Complementation test of the Arabidopsis CYP735A-deficient mutant and CK profiling of loss-of-function rice mutant, cyp735a3 cyp735a4, demonstrated that CYP735A3 and CYP735A4 encode P450s required for tZ-type side-chain modification in rice. CYP735As are expressed in both roots and shoots. The cyp735a3 cyp735a4 mutants exhibited growth retardation concomitant with reduction in CK activity in both roots and shoots, indicating that tZ-type CKs function in growth promotion of both organs. Expression analysis revealed that tZ-type CK biosynthesis is negatively regulated by auxin, abscisic acid, and cytokinin and positively by dual nitrogen nutrient signals, namely glutamine-related and nitrate-specific signals. These results suggest that the physiological role of tZ-type CKs in rice is different from that in Arabidopsis and they control growth of both roots and shoots in response to internal and environmental cues in rice.

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Nitrogen Nutrition Promotes Rhizome Bud Outgrowth via Regulation of Cytokinin Biosynthesis Genes and an Oryza longistaminata Ortholog of FINE CULM 1

Cited by 15 publications

References 30 publications

Regulation of ammonium acquisition and use in Oryza longistaminata ramets under nitrogen source heterogeneity

Regulation of ammonium acquisition and use in Oryza longistaminata ramets under nitrogen source heterogeneity

Transcriptome Analysis Reveals a Gene Expression Pattern That Contributes to Sugarcane Bud Propagation Induced by Indole-3-Butyric Acid

Thetrans-zeatin-type side-chain modification of cytokinins controls rice growth

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